Optical mapping of impulse propagation in engineered cardiac tissue

Tissue Engineering - Part A

Volumn 15, Issue 4, 2009, Pages 851-860

  Radisic, Milica ^a   Fast, Vladimir G ^b   Sharifov, Oleg F ^b   Iyer, Rohin K ^a   Park, Hyoungshin ^c,d   Vunjak Novakovic, Gordana ^e  

^a UNIVERSITY OF TORONTO   (Canada)

^b and Radiation Oncology   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d Massachusetts Institute of Technology Cambridge   (United States)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMIMETICS; BIOREACTORS; CELL CULTURE; CELL MEMBRANES; INDUSTRIAL CHEMICALS; TISSUE; TISSUE ENGINEERING;

AMPLITUDE OF CONTRACTIONS; CARDIAC CONSTRUCTS; CARDIAC TISSUE ENGINEERING; CARDIAC TISSUES; CELL DIFFERENTIATION; COLLAGEN SCAFFOLDS; CONDUCTION VELOCITY; CONTRACTILE BEHAVIOR; ELECTRICAL FIELD; ELECTRICAL IMPULSE; ELECTRICAL PROPAGATION; ELECTRICAL SIGNAL; ELECTRICAL STIMULATIONS; IN-VITRO; IN-VIVO; NEONATAL RAT; OPTICAL MAPPING; TISSUE CONSTRUCTS; TISSUE MORPHOLOGY;

ELECTRIC PROPERTIES;

COLLAGEN; CONNEXIN 43;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CONTROLLED STUDY; ELECTRIC FIELD; ELECTROSTIMULATION; GEL ELECTROPHORESIS; HEART MUSCLE; HEART MUSCLE CONTRACTILITY; MICROSCOPY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE ENGINEERING; VELOCITY; ANIMAL; BIOREACTOR; CELL CULTURE; CYTOLOGY; ELECTRIC CONDUCTIVITY; HEART; METABOLISM; METHODOLOGY; PHYSIOLOGY;

RATTUS;

ANIMALS; ANIMALS, NEWBORN; BIOREACTORS; CELLS, CULTURED; COLLAGEN; ELECTRIC CONDUCTIVITY; ELECTRIC STIMULATION; HEART; MYOCARDIUM; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE ENGINEERING;

EID: 67049137916     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2008.0223     Document Type: Article

References (46)

1. Krikpatrick, J.N., Vannan, M.A., Narula, J., and Lang, R.M. Echocardiography in heart failure: applications, utility, and new horizons. J Am Coll Cardiol 50, 381, 2007.
2. Radisic, M., Euloth, M., Yang, L., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. High-density seeding of myocyte cells for cardiac tissue engineering. Biotechnol Bioeng 82, 403, 2003.
3. Park, H., Radisic, M., Lim, J.O., Chang, B.H., and Vunjak- Novakovic, G. A novel composite scaffold for cardiac tissue engineering. In Vitro Cell Dev Biol Anim 41, 188, 2005.
4. Zong, X., Bien, H., Chung, C.Y., Yin, L., Fang, D., Hsiao, B.S., Chu, B., and Entcheva, E. Electrospun fine-textured scaffolds for heart tissue constructs. Biomaterials 26, 5330, 2005.
5. McDevitt, T.C., Woodhouse, K.A., Hauschka, S.D., Murry, C.E., and Stayton, P.S. Spatially organized layers of cardiomyocytes on biodegradable polyurethanefilms for myocardial repair. J Biomed Mater Res A 66, 586, 2003.
6. Carrier, R.L., Rupnick,M., Langer, R., Schoen, F.J., Freed, L.E., and Vunjak-Novakovic, G. Perfusion improves tissue architecture of engineered cardiac muscle. Tissue Eng 8, 175, 2002.
7. Boublik, J., Park, H., Radisic, M., Tognana, E., Chen, F., Pei, M., Vunjak-Novakovic, G., and Freed, L.E. Mechanical properties and remodeling of hybrid cardiac constructs made from heart cells, fibrin, and biodegradable, elastomeric knitted fabric. Tissue Eng 11, 1122, 2005.
8. Badylak, S.F., Kochupura, P.V., Cohen, I.S., Doronin, S.V., Saltman, A.E., Gilbert, T.W., Kelly, D.J., Ignotz, R.A., and Gaudette, G.R. The use of extracellular matrix as an inductive scaffold for the partial replacement of functional myocardium. Cell Transplant 15 Suppl 1, S29, 2006.
9. Zimmermann, W.H., Didie, M., Doker, S., Melnychenko, I., Naito, H., Rogge, C., Tiburcy, M., and Eschenhagen, T. Heart muscle engineering: an update on cardiac muscle replacement therapy. Cardiovasc Res 71, 419, 2006.
10. Eschenhagen, T., and Zimmermann, W.H. Engineering myocardial tissue. Circ Res 97, 1220, 2005.
11. Laflamme, M.A., and Murry, C.E. Regenerating the heart. Nat Biotechnol 23, 845, 2005.
12. Takahashi, K., and Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663, 2006.
13. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861, 2007.
14. Nakagawa, M., Koyanagi, M., Tanabe, K., Takahashi, K., Ichisaka, T., Aoi, T., Okita, K., Mochiduki, Y., Takizawa, N., and Yamanaka, S. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 26, 101, 2008.
15. Park, I.H., Zhao, R., West, J.A., Yabuuchi, A., Huo, H., Ince, T.A., Lerou, P.H., Lensch, M.W., and Daley, G.Q. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451, 141, 2008.
16. Lowry, W.E., Richter, L., Yachechko, R., Pyle, A.D., Tchieu, J., Sridharan, R., Clark, A.T., and Plath, K. Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc Natl Acad Sci USA 105, 2883, 2008.
17. Radisic, M., Yang, L., Boublik, J., Cohen, R.J., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. Medium perfusion enables engineering of compact and contractile cardiac tissue. Am J Physiol Heart Circ Physiol 286, H507, 2004.
18. Bursac, N., Loo, Y., Leong, K., and Tung, L. Novel anisotropic engineered cardiac tissues: studies of electrical propagation. Biochem Biophys Res Commun 361, 847, 2007.
19. Nag, A.C. Study of non-muscle cells of the adult mammalian heart: a fine structural analysis and distribution. Cytobios 28, 41, 1980.
20. Banerjee, I., Yekkala, K., Borg, T.K., and Baudino, T.A. Dynamic interactions between myocytes, fibroblasts, and extracellular matrix. Ann NY Acad Sci 1080, 76, 2006.
21. Kuzuya, M., and Kinsella, J.L. Induction of endothelial cell differentiation in vitro by fibroblast-derived soluble factors. Exp Cell Res 215, 310, 1994.
22. Seghezzi, G., Patel, S., Ren, C.J., Gualandris, A., Pintucci, G., Robbins, E.S., Shapiro, R.L., Galloway, A.C., Rifkin, D.B., and Mignatti, P. Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J Cell Biol 141, 1659, 1998.
23. Naito, H., Melnychenko, I., Didie, M., Schneiderbanger, K., Schubert, P., Rosenkranz, S., Eschenhagen, T., and Zimmermann, W.H. Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114, I72, 2006.
24. Radisic, M., Park, H., Martens, T.P., Salazar-Lazaro, J.E., Geng, W., Wang, Y., Langer, R., Freed, L.E., and Vunjak- Novakovic, G. Pre-treatment of synthetic elastomeric scaffolds by cardiac fibroblasts improves engineered heart tissue. J Biomed Mater Res A 2007.
25. Radisic, M., Park, H., Shing, H., Consi, T., Schoen, F.J., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci USA 101, 18129, 2004.
26. Fast, V.G., and Cheek, E.R. Optical mapping of arrhythmias induced by strong electrical shocks in myocyte cultures. Circ Res 90, 664, 2002.
27. Fast, V.G. Recording action potentials using voltagesensitive dyes. In: Dhein, S., Delmar, M., and Mohr, F.W., eds. Methods in Cardiovascular Research. Berlin: Springer- Verlag, 2005, p. 233-255.
28. Radisic, M., Park, H., Chen, F., Salazar-Lazzaro, J.E., Wang, Y., Dennis, R., Langer, R., Freed, L.E., and Vunjak- Novakovic, G. Biomimetic approach to cardiac tissue engineering: oxygen carriers and channeled scaffolds. Tissue Eng 12, 2077, 2006.
29. Radisic, M., Marsano, A., Maidhof, R., Wang, Y., and Vunjak-Novakovic, G. Cardiac tissue engineering using perfusion bioreactor systems. Nature Protocols 3, 719, 2008.
30. Bursac, N., Papadaki, M., Langer, R., Eisenberg, S.R., Vunjak- Novakovic, G., and Freed, L.E. Towards a functional tissue engineered cardiac muscle. 21st Annual Meeting of the Biomedical Engineering Society, Atlanta, 1999, p. 29.
31. Sun, L.S., Legato, M.J., Rosen, T.S., Steinberg, S.F., and Rosen, M.R. Sympathetic innervation modulates ventricular impulse propagation and repolarisation in the immature rat heart. Cardiovasc Res 27, 459, 1993.
32. Zimmermann, W.H., Melnychenko, I., Wasmeier, G., Didie, M., Naito, H., Nixdorff, U., Hess, A., Budinsky, L., Brune, K., Michaelis, B., Dhein, S., Schwoerer, A., Ehmke, H., and Eschenhagen, T. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12, 452, 2006.
33. Carrier,R.L., Papadaki,M.,Rupnick,M., Schoen,F.J., Bursac,N., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. Cardiac tissue engineering: cell seeding, cultivation parameters and tissue construct characterization. Biotechnol Bioeng 64, 580, 1999.
34. Bursac, N., Papadaki, M., Cohen, R.J., Schoen, F.J., Eisenberg, S.R., Carrier, R., Vunjak-Novakovic, G., and Freed, L.E. Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies. Am J Physiol Heart Circ Physiol 277, H433, 1999.
35. Fink, C., Ergun, S., Kralisch, D., Remmers, U., Weil, J., and Eschenhagen, T. Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J 14, 669, 2000.
36. Papadaki, M., Bursac, N., Langer, R., Merok, J., Vunjak-Novakovic, G., and Freed, L.E. Tissue engineering of functional cardiac muscle: molecular, structural and electrophysiological studies. Am J Physiol Heart Circ Physiol 280, H168, 2001.
37. Zimmermann, W.H., Schneiderbanger, K., Schubert, P., Didie, M., Munzel, F., Heubach, J.F., Kostin, S., Nehuber, W.L., and Eschenhagen, T. Tissue engineering of a differentiated cardiac muscle construct. Circ Res 90, 223, 2002.
38. Iyer, R., Chiu, L., and Radisic, M. Microfabricated poly(ethylene glycol) templates enable rapid screening of triculture conditions for cardiac tissue engineering. J Biomed Mater Res Part A, 2008. [Epub ahead of print]
39. Boateng, S.Y., Hartman, T.J., Ahluwalia, N., Vidula, H., Desai, T.A., and Russell, B. Inhibition of fibroblast proliferation in cardiac myocyte cultures by surface microtopography. Am J Physiol Cell Physiol 285, C171, 2003.
40. Shen, Y.H., Shoichet, M.S., and Radisic, M. Vascular endothelial growth factor immobilized in collagen scaffold promotes penetration and proliferation of endothelial cells. Acta Biomater 4, 477, 2008.
41. Sun, Y., Kiani, M.F., Postlethwaite, A.E., and Weber, K.T. Infarct scar as living tissue. Basic Res Cardiol 97, 343, 2002.
42. Miragoli, M., Gaudesius, G., and Rohr, S. Electrotonic modulation of cardiac impulse conduction by myofibroblasts. Circ Res 98, 801, 2006.
43. Cannizzaro, C., Tandon, N., Figallo, E., Park, H., Gerecht, S., Radisic, M., Elvassore, N., and Vunjak-Novakovic, G. Practical aspects of cardiac tissue engineering with electrical stimulation. Methods Mol Med 140, 291, 2007.
44. Tandon, N., Cannizzaro, C., Chao, G., Maidhof, R., Marsano, A., Au, H., Radisic, M., and Vunjak-Novakovic, G. Electrical stimulation systems for cardiac tissue engineering. Nat Protoc [in press].
45. Yeo, Y., Geng, W., Ito, T., Kohane, D.S., Burdick, J.A., and Radisic, M. Photocrosslinkable hydrogel for myocyte cell culture and injection. J Biomed Mater Res B Appl Biomater 81, 312, 2007.
46. Gerecht, S., Burdick, J.A., Ferreira, L.S., Townsend, S.A., Langer, R., and Vunjak-Novakovic, G. Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stemcells. ProcNatlAcad Sci USA104, 11298, 2007.